The cognitive level does not interfere with recovery after robot-assisted gait training in traumatic brain injury: A 10-year cohort study

Abstract

BACKGROUND:

There is still no clear evidence available on the role of robot-assisted gait training (RAGT) in severe traumatic brain injury (TBI) and on the relationship between this intervention and cognitive impairment.

OBJECTIVE:

This study investigates the impact of the cognitive level at admission on functional recovery in a cohort of patients with severe TBI who received RAGT training within a multidisciplinary rehabilitation setting.

METHODS:

We included patients with gait disturbance due to a severe TBI. Patients were grouped into three classes according to their level of cognitive functioning (LCF) at admission (LCF 2-3; LCF 4-5-6; LCF 7-8). We collected demographics (sex, age), clinical data, and a set of outcome measures at admission and discharge.

RESULTS:

We registered 80 patients, 19 females and 61 males, 35.3 $\pm$ 14.85 years. Patients with a low cognitive level at admission were mostly subacute ( $p=$ 0.001). Cognitive impairment despite longer length stay in the hospital (LOS) ( $p=$ 0.001) did not preclude recovery after RAGT in terms of cognition ( $R^{2}=$ 0.68; $p<$ 0.0001), functional independence ( $R^{2}=$ 0.30; $p<$ 0.0001) and overall disability ( $R^{2}=$ 0.32; $p<$ 0.0001).

CONCLUSION:

Irrespective of their level of cognition, patients with severe TBI might benefit from RAGT during a multidisciplinary program.

Keywords

Traumatic brain injury robot-assisted gait training cognition multidisciplinary rehabilitation disability

1. Introduction

Traumatic brain injury (TBI) is a common cause of neurological damage and disability that affects the medical, social and economic spheres. To date, according to recent epidemiological studies, TBI incidence rate in Europe is estimated between 83.3 and 849 per 100.000 of the population per year (regional-level studies) [1]. Cognitive impairment is usually also a consequence of brain trauma. Cognitive sequelae were reported in about 65% of patients, and physical sequelae in 40% of patients in the case of moderate and severe TBIs. Even in cases of mild TBI without visible physical sequelae, 43% of people suffer from cognitive impairments [2, 3]. The parts of the brain that are most commonly affected in traumatic brain injuries are the frontal and temporal lobes [4]; the frontal lobe is considered the crucial neural substrate for cognitive and social behaviour. For this reason, the cognitive assessment of patients following a severe TBI is mandatory [3].

Pilot studies have shown that patients with TBI have good cognitive and functional recovery through rehabilitation, especially young patients in the acute phase [5, 6]. Other studies have shown a high correlation between cognitive recovery and functional improvement in these patients [6, 7]. The past two decades have seen the introduction of new rehabilitation interventions that are based on the use of robotics. RAGT is intended to allow the patient to practice more ‘normal’ gait patterns. Robotic exoskeletons can provide the user with intensive, goal-directed movement repetition and stability and balance during gait, compared to conventional physical therapy. Robot-assisted therapy helps patients to accelerate functional recovery [8, 9]. The use of robotic technology combined with multidisciplinary rehabilitation is an added value that improves patients’ mobility and allows health professionals to organise their work better [10, 11, 12].

Moreover, RAGT can improve the gait pattern and increase the volume of patients’ activity while reducing the therapist’s physical burden, and contribute to shortening the duration of hospitalization [13]. So far, studies have reported a potential beneficial effect of RAGT in patients with TBI, both in terms of walking function and of gait symmetry [8, 11, 14]. Moreover, this intervention seems safe and feasible even in patients with severe TBI with disorders of consciousness [11]. Thus, so far, RAGT can be considered an option for delivering an-high-intensity walking training to restore functional abilities within a multidisciplinary rehabilitation program. However, no clear information on cognitive disorders’ impact on recovery in patients with severe traumatic brain injury who receive RAGT is available. The aim of this observational study is to investigate the influence of the cognitive level at admission on a variety of outcomes, including disability, walking function, cognitive level, and independence of daily living in a cohort of patients with severe traumatic brain injury who received RAGT within the context of multidisciplinary rehabilitation.

2. Materials and methods

We retrospectively analysed a database that includes patients with severe TBI admitted to an inpatient multidisciplinary rehabilitation programme of the University of Ferrara and received robot-assisted gait rehabilitation between January 2007 and December 2017. The ethics committee approved the study, but written informed consent was not collectable from all patients since part of them was no longer attending the rehabilitation clinics.

2.1 Subjects

The criteria of inclusion for the study were: (i) male or female aged over 18; (ii) severe or moderate traumatic brain injury (TBI) according to the Glasgow Coma Scale (GCS) [15]. Patients with medical instability, aggressive behaviour and skin lesions were excluded from the use of RAGT. We collected the following demographic and clinical data: age; (2) sex; (3) Glasgow Outcome Scale Extended (GOSE) at admission and discharge; (4) physical limitations (paraosteoarthropathy, limb fractures, spasticity); (5) Level of Cognitive Functioning (LCF) at admission and discharge; (6) motor impairment (right hemiplegia, left hemiplegia, tetraplegia, motor disorders); (7) rehabilitation phase (sub-acute, defined as $<$ 6 months and chronic, defined as $>$ 6 months from the acute event); (8) Functional independence measure (FIM): total score (tFIM), motor subscore (mFIM) and cognitive subscore (cFIM) at admission and discharge; (9) Functional Ambulatory Classification (FAC) at admission and discharge. Moreover, a set of measures related to rehabilitation training protocol were collected, including (i) the length of stay in the hospital (LOS), (ii) the number of RAGT sessions, (iii) the period since the TBI event and RAGT training.

Our analysis focused on the impact of the cognitive level at admission measured by the Level of Cognitive Functioning (LCF) score. It is a scale used to classify cognitive and behavioural disorders caused by TBI. It is structured in eight levels, characterizing the level of cognitive damage from a coma to the full recovery of consciousness [16, 17]. We divided our sample into three main classes according to their LCF level at rehabilitation admission. The first group includes patients with disorders of consciousness that are scored as LCF 2 or 3; the second group is characterized by patients with moderate to severe cognitive and behavioural disorders (LCF score of 4, 5 and 6); the third group presents mild to moderate cognitive and behavioural disorders (LCF score 7 and 8).

2.2 Interventions

All patients of the program received robot-assisted gait rehabilitation. RAGT was performed using a robotic exoskeleton system (Lokomat: Hocoma, Switzerland) to guide hip and knee flexion through braces connecting the patient’s legs to the machine. It also provides bodyweight support (0–100%) through a harness, along with the level of assistance provided by the device. The entire device (including the harness and the motorized exoskeleton orthoses) can be adjusted according to the requirements of treadmill rehabilitation. Motorized exoskeleton orthoses have a biomechanical role, guiding movements at the hips and knees that mimic a physiological gait pattern [18]. Parameters are defined based on the functional characteristics of the patient, starting with a 50% reduction in body weight and 100% of the guidance provided by the robot. Over the sessions, adjustments can be made in increments or decrements of 10%. The RAGT session lasts approximately 45 minutes to an hour, including patient preparation. The treadmill speed can vary from 0.1 to 3 km/h [19]. In addition to RAGT, patients benefited from a multidisciplinary rehabilitation programme defined according to the individual’s needs (conventional motor rehabilitation, occupational therapy, speech therapy and cognitive rehabilitation).

2.3 Multidisciplinary rehabilitation

The inpatient TBI rehabilitation program delivered medical and rehabilitation treatments by a multidisciplinary team to help patients regain their independence and better living conditions. Among these treatments, we distinguish occupational, speech, physical, psychological and neurocognitive therapy; all these treatments were selected on specific individual needs.

At the admission, the patient was assessed by a rehabilitation team who defined a specific program according to the WHO International Classification of Functioning [20, 21]. At discharge, a clinical evaluation was made to determine the functional improvement of patients.

2.4 Statistical analysis

We completed statistical comparisons for each of the demographic and clinical parameters mentioned above. The analysis is based on the Kruskal Wallis rank test for continuous variables and the Chi-Square value for categorical variables. Correlations among variables were tested with the Spearman correlation coefficient (rho), and linear regression models were used to test the impact of cognitive status ad admission on functional recovery. A significance level of $p<$ 0.05 was set.

3. Results

We included 80 participants with TBI: 19 (23.75%) were females (34.55 $\pm$ 14.59 years old), and 61 (76.25%) were male (35.82 $\pm$ 15.23 years old). The three classes (LCF 2-3, LCF 4-6, LCF 7-8) were comparable for sex, physical limitations (limb fractures, spasticity, paraosteoarthropathy) and motor impairment (right hemiplegia, left hemiplegia, tetraplegia). Conversely, we observed differences across the groups with respect to age ( $p=$ 0.024), GCS score ( $p=$ 0.005), phase of rehabilitation ( $p=$ 0.001) and clinical outcome (FAC, LCF, GOSE, tFIM score, mFIM, cFIM) ( $p=$ 0.001). Specifically, the more cognitive impaired group (LCF 2-3) was younger, with a lower GCS score after the TBI, was mostly admitted for rehabilitation in the subacute phase and presented poorer clinical score at admission. Differences among groups were highlighted even considering when RAGT was delivered with respect to the admission to the rehabilitation ( $p=$ 0.001). The LCF 2-3 group received RAGT later compared to the other groups during their rehabilitation stay. See Table 1.

Table 1
Sample demographics and clinical characteristics

	LCF 2-3 ( $n=$ 24)	LCF 4-6 ( $n=$ 42)	LCF 7-8 ( $n=$ 14)	Total ( $n=$ 80)	$p$
Age	29.83 (14.77)	37.87 (15.09)	37.21 (12.43)	35.32 (14.84)	0.024
Sex (F/M)	8/16	6/36	5/9	19/61	0.192
GCS score	4.33 (1.73)	5.78 (2.03)	6.78 (2.63)	5.52 (2.22)	0.004
Rehabilitation phase					0.001
Subacute	18	18	1	37
Chronic	6	24	13	43
Physical limitations					0.210
Limb fractures	8	15	4	27
Spasticity	14	20	6	40
POA	1	7	2	10
Motor impairment					0.546
Right hemiplegia	5	7	1	13
Left hemiplegia	4	9	3	16
Tetraplegia	13	22	6	41
Movement disorders	2	4	4	10
LCF	2.5 (0.51)	5.19 (0.74)	7 (0.00)	4.7 (1.7)	0.001
GOSE	2.37 (0.49)	3.45 (0.8)	4.21 (0.58)	3.26 (0.94)	0.001
FAC	0.17 (0.64)	0.67 (1.12)	2.78 (1.25)	0.88 (1.36)	0.001
tFIM	18.58 (2.04)	41.95 (23.3)	63.71 (17.47)	28.38 (22.74)	0.001
mFIM	13.12 (0.45)	25.33 (18.09)	63.71 (17.47)	28.38 (22.74)	0.001
cFIM	6.04 (3.02)	16.52 (7.66)	31.86 (3.93)	16.06 (10.1)	0.001
Rehab-RAGT (days)	100 (78)	52 (50)	23 (27)	61 (63)	0.001
RAGT (sessions)	17.66 (11.6)	17.13 (9.45)	12.92 (5.61)	16.65 (9.78)	0.397
LOS (days)	184.55 (92.49)	157.44 (99.71)	73.30 (38.30)	153.18 (96.84)	0.001

GCS $=$ Glasgow Coma Scale; POA $=$ paraosteoarthropathy; LCF $=$ Level of Cognitive Functioning; GOSE $=$ Glasgow Outcome Scale Extended; FAC $=$ Functional Ambulatory classification; FIM $=$ Functioning Independence Measure: tFIM (total score), mFIM (motor domain), cFIM (cognitive domain). RAGT $=$ Robot-Assist Gait Training, LOS $=$ Length of Stay.

The analysis showed that participants with a lower cognitive level at admission were mostly in the subacute phase of rehabilitation ( $p=$ 0.001) and had a better functional recovery. Specifically, we found an improvement not only with regards to cognition ( $p=$ 0.001), but also in walking function ( $p=$ 0.037), independence of daily living ( $p=$ 0.001), and disability ( $p=$ 0.034). These findings were not statistically different in subacute and chronic subgroups, except for cognition ( $p=$ 0.0001). See Table 2.

Table 2

Functional improvements according with cognition level at admission and rehabilitation phase

		LCF 2-3 ( $n=$ 24)	LCF 4-6 ( $n=$ 42)	LCF 7-8 ( $n=$ 14)	Total ( $n=$ 80)	$p$
DLCF	Subacute	3.56 (1.25)	1.29 (0.77)	0 (0.1)	2.35 (1.52)	0.001
	Chronic	2 (1.1)	0.58 (0.72)	0 (0)	0.60 (0.9)	0.0018
	Total	3.16 (1.37)	0.88 (0.80)	0.00 (0.00)	1.41 (1.52)	0.001
DGOSE	Subacute	2.56 (1.5)	1.6 (0.98)	1 (0.1)	2.1 (1.3)	0.120
	Chronic	1.67 (1.51)	0.42 (0.78)	0.23 (0.44)	0.53 (0.93)	0.0495
	Total	2.33 (1.17)	0.92 (0.77)	0.34 (0.47)	1.24 (1.36)	0.034
DFAC	Subacute	2.44 (1.5)	1.89 (1.53)	2 (0.1)	2.16 (1.5)	0.470
	Chronic	1 (0.6)	0.71 (0.62)	0.92 (0.64)	0.81 (0.63)	0.532
	Total	2.08 (1.47)	1.21 (1.24)	1 (0.68)	1.43 (1.30)	0.037
DtFIM	Subacute	57.06 (29.46)	45.11 (25.14)	23 (0.1)	50.32 (27.67)	0.220
	Chronic	26.83 (22.78)	9.25 (9.63)	7.31 (8.01)	11.12 (13.14)	0.168
	Total	49.5 (30.54)	24.62 (25.23)	8.43 (8.76)	29.25 (28.76)	0.001
DmFIM	Subacute	39 (24.15)	33.83 (21.24)	21 (0.1)	36 (22.39)	0.620
	Chronic	18.33 (18.4)	6.17 (6.56)	7 (7.44)	8.12 (9.86)	0.240
	Total	33.83 (24.25)	18.02 (20.27)	8.96 (8.06)	21.01 (21.81)	0.001
DcFIM	Subacute	17.94 (7.53)	11.22 (6.86)	2 (0.1)	14.24 (8.04)	0.012
	Chronic	8.5 (6.28)	3.08 (4.54)	0.31 (0.63)	3 (4.76)	0.0163
	Total	15.58 (8.24)	6.57 (6.90)	0.43 (0.75)	8.2 (8.56)	0.001

LCF $=$ Level of Cognitive Functioning; GOSE $=$ Glasgow Outcome Scale Extended; FAC $=$ Functional Ambulatory classification; FIM $=$ Functioning Independence Measure: tFIM (total score), mFIM (motor domain), cFIM (cognitive domain).

Evidence of greater gains was demonstrated in patients in the subacute rather than chronic rehabilitation phase in all clinical outcomes: LCF ( $p=$ 0.001); GOSE ( $p=$ 0.003); FAC ( $p=$ 0.038) and FIM ( $p=$ 0.001). See Fig. 1.

Figure 1.

Clinical variation in function of rehabilitation phase.

The level of cognitive function at admission was strongly correlated with the increase in the level of cognitive function at discharge (rho $=$ $-$ 0.83; $p=$ 0.001), moderately with $\Delta$ GOSE (rho $=$ $-$ 0.57; $p=$ 0.001), $\Delta$ tFIM (rho $=$ $-$ 0.56; $p=$ 0.001), $\Delta$ cFIM (rho $=$ $-$ 0.65; $p=$ 0.001) fair with $\Delta$ mFIM (rho $=$ $-$ 0.46; $p=$ 0.001) and $\Delta$ FAC (rho $=$ $-$ 0.33; $p=$ 0.003). We concluded that the level of cognition at admission can explain the 68.15% of the cognitive improvement ( $R^{2}=$ 0.68; $\beta=$ $-$ 0.74, $p=$ 0.001); 32.74% of the disability improvement ( $R^{2}=$ 0.33; $\beta=$ $-$ 0.34, $p=$ 0.001); 30% of functional ability improvement ( $R^{2}=$ 0.3; $\beta$ $=$ $-$ 9.31, $p=$ 0.001) including 22% motor and 42% cognitive ability, and also responsible for 11% of the improvement in gait ( $R^{2}$ $=$ 0.11; $\beta=$ $-$ 0.25, $p=$ 0.003). See Table 3.

Table 3

Impact of the cognitive level at admission on functional recovery

	DF	rho	R-square	$B$	$t$	$P$
DGOSE	79	$-$ 0.5680	0.3274	$-$ 0.337	$-$ 6.16	0.000
DFAC	79	$-$ 0.3290	0.1081	$-$ 0.251	$-$ 3.07	0.003
DLCF	79	$-$ 0.8259	0.6815	$-$ 0.740	$-$ 12.92	0.000
DtFIM	79	$-$ 0.5558	0.3033	$-$ 9.310	$-$ 5.83	0.000
DmFIM	79	$-$ 0.4584	0.2159	$-$ 5.956	$-$ 4.63	0.000
DcFIM	79	$-$ 0.6520	0.4259	$-$ 3.283	$-$ 7.61	0.000

R-Square $=$ coefficient of determination; DF $=$ degree of freedom; $B=$ slope of regression; $p=$ probability; rho $=$ coefficient of correlation; rho: coefficient of correlation.

Patients with disorders of consciousness have had a longer period to recover and to receive RAGT. Specifically, patients with a lower level of cognition needed a longer rehabilitation stay and time to receive RAGT ( $p=$ 0.001). The total number of RAGT sessions did not influence the level of consciousness of different patients ( $p=$ 0.397) (Table 1). Moreover, a weak correlation has been observed between RAGT sessions and FIM recovery (rho $=$ 0.2).

4. Discussion

The sequelae resulting from a severe TBI are not only those related to functional but also cognitive, mental and emotional aspects. For this reason, all these elements must be considered by the rehabilitation processes [22, 23, 24]. This work aimed to produce a comprehensive analysis using demographic and clinical parameters to investigate the impact of the cognitive level at admission on RAGT and the functional recovery in terms of walking independence, cognitive level, independence of daily living and disability. The influence of cognitive disorders on the efficacy of RAGT within a multidisciplinary rehabilitation inpatient program for TBI survivors has not been previously established [9, 12, 13].

Regarding the outcomes observed, patients with disorders of consciousness at admission had a more remarkable improvement, particularly in cognitive function. However, we noticed that they were relatively younger (under 30 years old), and age is a significant factor in functional recovery during TBI rehabilitation [25, 26, 27]. Several studies have shown the ability of young patients to integrate new knowledge and learning skills [5, 27]. Moreover, patients with disorders of consciousness had lower GCS scores, reflecting a more significant brain injury severity. This aspect justifies the longer rehabilitation length of stay and time between the event and RAGT training [28].

In addition, we observed a substantial difference concerning the phase of rehabilitation. As previously highlighted, patients who receive RAGT during a multidisciplinary rehabilitation in the subacute phase of recovery had a more favourable outcome in functional recovery [12].

In our TBI sample, most of the patients with disorders of consciousness were in their first six months since injury (75%), instead of the others (41.85 and 7.13%), and this difference might have influenced the results. The disorder of consciousness seems not to be an obstacle to the application of RAGT within a multidisciplinary rehabilitation program, as previously reported [11, 23, 30]. Considering the training intensity, our TBI cohort received more sessions compared to previous work [11], without any significant differences among LCF scores.

In our cohort, the cognitive level at admission influenced the rehabilitation length of stay (LOS) and the time needed to receive RAGT during the multidisciplinary rehabilitation program. As previously reported, patients with disorders of consciousness need an extended period to recover. Similarly, a longer period to receive RAGT safely was necessary [32, 33, 34, 35].

This observational study has several limitations. Firstly, the study design does not permit establishing a direct cause-effect relationship between the cognitive level and functional improvement after RAGT in patients with severe TBI. Secondly, the combination of RAGT and a multidisciplinary rehabilitation program tailored to the patients’ rehabilitation needs prevent us from discriminating between the effects of the two different treatment modalities. This study suggests further analysis by prospective and clinical studies to understand better the impact of the cognitive level on functional recovery in patients with severe TBI who receive RAGT within an inpatient multidisciplinary rehabilitation program.

5. Conclusion

Robot-assisted gait training within an inpatient multidisciplinary rehabilitation program was feasible and safe in patients with severe TBI who improved their walking function, cognition and functional independence. These results were irrespective of their level of cognition.

However, the cognitive level affected the rehabilitation length of stay and the time needed to receive RAGT during the multidisciplinary rehabilitation program.

Author contributions

CONCEPTION: Luc Oscar Lissom, Sofia Straudi and Valentina Bonsangue

PERFORMANCE OF WORK: Luc Oscar Lissom, Valentina Bonsangue and Marina Macca

INTERPRETATION OR ANALYSIS OF DATA: Luc Oscar Lissom, Sofia Straudi and Giacomo Severini

PREPARATION OF THE MANUSCRIPT: Luc Oscar Lissom, Sofia Straudi, Valentina Bonsangue and Marina Macca

REVISION FOR IMPORTANT INTELLECTUAL CONTENT: Valentina Bonsangue, Marina Macca, Giacomo Severini, Susanna Lavezzi and Nino Basaglia

SUPERVISION: Luc Oscar Lissom, Valentina Bonsangue, Marina Macca, Giacomo Severini, Susanna Lavezzi, Nino Basaglia and Sofia Straudi

Ethical considerations

This study was approved by the Ferrara Ethics Comittee.

Footnotes

Acknowledgments

The authors have no acknowledgments.

Conflict of interest

The authors have no conflicts of interest to report.

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The cognitive level does not interfere with recovery after robot-assisted gait training in traumatic brain injury: A 10-year cohort study

Abstract

BACKGROUND:

OBJECTIVE:

METHODS:

RESULTS:

CONCLUSION:

Keywords

1. Introduction

2. Materials and methods

2.1 Subjects

2.2 Interventions

2.3 Multidisciplinary rehabilitation

2.4 Statistical analysis

3. Results

Table 1 Sample demographics and clinical characteristics

5. Conclusion

Author contributions

Ethical considerations

Footnotes

Acknowledgments

Conflict of interest

References

Table 1
Sample demographics and clinical characteristics